Deciphering the processes driving the evolution of the diverse pheromone-mediated chemical communication system of insects is a fascinating and challenging task. Understanding how pheromones have arisen has been supported by studies with the model organism Leptopilina heterotoma, a parasitoid wasp whose defensive compound (-)-iridomyrmecin also evolved as a component of the female sex pheromone and as a cue to avoid competition with other females during host search. To understand how compounds can evolve from being non-communicative to having a communicative function and to shed light on the evolution of the multi-functional use of iridomyrmecin in the genus Leptopilina, the chemical communication of two additional species, L. ryukyuensis and L. japonica, was studied. We demonstrate that in both species a species-specific mixture of iridoids is produced and emitted by wasps upon being attacked, consistent with their putative role as defensive compounds. In L. ryukyuensis these iridoids are also used by females to avoid host patches already exploited by other conspecific females. However, females of L. japonica do not avoid the odor of conspecific females during host search. We also show that the sex pheromone of female L. ryukyuensis consists of cuticular hydrocarbons (CHCs), as males showed strong courtship behavior (wing fanning) towards these compounds, but not towards the iridoid compounds. In contrast, males of L. japonica prefer their females' iridoids but CHCs also elicit some courtship behavior. The use of iridoid compounds as defensive allomones seems to be common in the genus Leptopilina, while their communicative functions appear to have evolved in a species-specific manner.